Effect of Insecticides on Natural-Enemies

Pesticides management options for control of invertebrate pests in many parts of the world. Despite an increase in the use of pesticides, crop losses due to pests have remained largely unchanged for 30–40 years. Beyond the target pests, broad-spectrum pesticides may affect non-target invertebrate species, including causing reductions in natural enemy population abundance and activity, and competition between pest species. Assays of invertebrates against weathered residues have shown the persistence of pesticides might play an important part in their negative impacts on natural enemies in the field. A potential outcome of frequent broad-spectrum pesticide use is the emergence of pests not controlled by the pesticides but benefiting from reduced mortality from natural enemies and competitive release, commonly known as secondary pests.


Introduction
Pesticides management options for control of invertebrate pests in many parts of the world [1, 2]. Despite an increase in the use of pesticides, crop losses due to pests have remained largely unchanged for 30-40 years [3]. Beyond the target pests, broad-spectrum pesticides may affect non-target invertebrate species [4], including causing reductions in natural enemy population abundance and activity [5,6], and competition between pest species [7]. Assays of invertebrates against weathered residues have shown the persistence of pesticides might play an important part in their negative impacts on natural enemies in the field [8].
A potential outcome of frequent broad-spectrum pesticide use is the emergence of pests not controlled by the pesticides but benefiting from reduced mortality from natural enemies and competitive release, commonly known as secondary pests [9][10][11]. Secondary pest outbreaks are challenging as they may also be caused by other mechanisms, which inherently make it difficult to determine how frequently pesticide use results in this outcome [10]. In cotton fields, it was estimated that 20% of late-season pesticide costs were attributable to secondary pest outbreaks caused by early-season pesticide applications for Lygus pests [10]. Higher numbers of cotton aphids, Aphis gossypii Glover and spider mites, Tetranychus urticae Koch were found in cotton fields that received early-season applications of insecticides against Helicoverpa spp. [5, 6].
One standardized approach for assessing non-target impacts of pesticides is the International Organization for Biological and Integrated Control-Pesticides and Beneficial Organisms (IOBC) rating system [12][13][14]. Subsequently, more bioassays

Systemic insecticides
Applied as granules have been promoted to be relatively non-toxic to natural enemies [49][50][51]. However, insecticides as systemic effect exhibit indirect effects against natural enemies via several mechanisms of prey floral parts contaminated with the active ingredients [52][53][54]. Systemic insecticides may indirectly influence natural enemies if the mortality of prey populations is high [55,56].
Natural enemies decrease the populations during starvation or dispersal [55,[57][58][59]]. This effect depends on the foraging efficiency of the specific natural enemy. Decrease quantity or density of available prey or decrease their quality such that they are not acceptable as a food source, indirectly affected on larvae and adults or female parasitoids not lay eggs. Reproduction, foraging, fecundity, and longevity [33].
The active ingredient of systemic insecticide is distributed into flower parts indirectly impact natural enemies that feed on plant pollen or nectar such as minute pirate bug, Orius spp., which feed on plants during their

Fenoxycarb
It is a juvenile hormone analog [80,81] that has shown to be indirectly harmful to some natural enemies. It is delay development time from of pupae and adult of C. rufilabris [81], also, delay development of third instar larvae but not first instar larvae. Also, reproduction of females is inhibiting when second and third instars were initially exposed to it [82,83]. Also, the same result against third instar larvae of C. carnea [84]. Also, happened indirect affect against female longevity and fecundity of, Micromus tasmaniae [74].

Cyromazine
It is a growth regulator that disrupts molting, it is affecting cuticle sclerotization during increasing cuticle stiffness [65], and exhibits indirect effects on the reproduction of Phytoseiulus persimilis [74], no indirect effect, against rates of adult  [92] or inhibits the reproduction of females of, P. persimilis [74]. Also, no indirect affect on oviposition and foraging of some parasitoids as Eretmocerus sp., and Encarsia luteola [90,93]. Insect growth regulators are susceptible to early instars [90, 94,95].
Indirect effects on natural enemies due to the volatility of the compound as it is known to be volatile and display vapor activity on some insect pests [98].
First larvae of Harmonia axyridis, exhibit increase of development time, also, no indirect effect on adult fecundity [106-108].

Selective feeding blockers
It is include flonicamid and pymetrozine, inhibits feeding activity of piercingsucking insects after initial insertion of their stylets into plant tissues and interfere with neural regulation of fluid intake through the mouthparts resulting in starvation [102,[109][110][111][112]. Flonicamid and pymetrozine, did not affect the development time, fertility, and parasitism of natural enemies, Episyrphus balteatus, Bembidion lampros; Aphidius rhopalosiphi, Adalia bipunctata; and Aleochara bilineata [112]. Pymetrozine exhibited minimal indirect effects on the reproduction of N. californicus [104]. Flonicamid did not indirectly affect parasitism, the sex ratio, and adult emergence of the parasitoid, L. dactylopii. Overall, minimal research has been conducted to determine the indirect effects of these types of pesticides on natural enemies [113].

Microbials
Entomopathogenic fungi and bacteria are, in general, not indirectly harmful to natural enemies, this may vary depending on concentration, natural enemy type, life stage exposed, the timing of application, and environmental conditions [114,115].
Indirect effect not be associated with entomopathogenic fungi or bacteria [116]. B. thuringiensis has been indirect effects on some parasitoids this is depended on the formulation [117].
Natural enemies ingest fungal spores during grooming or feeding on contaminated hosts [89]; also, indirect effects depend on the concentration of spores [118]. Entomopathogenic fungi indirectly affect some natural enemies during feeding on prey that have been sprayed. Larvae of, Cryptolaemus montrouzieri were killed (50% mortality) after consuming mealybugs that had been sprayed with Beauveria bassiana [115]. B. bassiana decreased the fecundity of N. californicus females [104]. Fungus Cephalosporium lecanii exhibited no indirect effects on the longevity of the leafminer parasitoid, Diglyphus begini [119]. Exposure to Metarhizium anisopliae had no indirect effect on prey consumption (fungus gnat larvae) of rove beetle, A. coriaria adults [101]. Exposure to Isaria (=Paecilomyces) fumosoroseus at low relative humidity (55%) resulted in no indirect effects on foraging behavior and longevity of the aphid parasitoid, Aphelinus asychis whereas both parameters were significantly reduced when exposed to a high (≥95%) relative humidity, which could impact the ability of the parasitoid to regulate aphid populations. Ovipositing females may avoid prey that is infected by entomopathogenic fungi [114].
Spinosad has been demonstrated to be indirectly harmful to a variety of predatory insects such as, C. carnea [120]; Hippodamia convergens; Orius laevigatus, Geocoris punctipes; and Nabis sp. [121,122]. Exposure to spinosad extended development time from the first instar to adult and decreased fertility of Harmonia axyridis females. Nevertheless, exposure to spinosad did not inhibit foraging behavior and reproduction of P. persimilis females [123,124]. Parasitoids may be indirectly affected by spinosad based on decreased reproduction and reduced longevity [125,126].

Miticides
It is like other pesticides, demonstrate variability in regards to any indirect effects against natural enemies depending on the type of miticide and predatory mite species [127]. It did not affect Neoseiulus (=Amblyseius) womersleyi on Tetranychus urticae, eggs [127,128]. Exposure to concentrations of fenpyroximate indirectly affect on longevity and fecundity of P. plumifer [129]. Pyridaben inhibited reproduction of Galendromus occidentalis [130]. No indirect effects associated with sex ratio and prey consumption of P. persimilis [131,132].
Exposure to bifenazate did not reduce fecundity, longevity, or prey consumption of P. persimilis or N. californicus [133].

Fungicides
It is considered low harmful to natural enemies comparing with insecticides and miticides [134]. Mancozeb was negatively affected against fecundity and reproduction of, Amblyseius andersoni, G. occidentalis [135], and Euseius victoriensis and inhibited the reproduction of, Amblyseius fallacis [130,136]. Also, it did not

Additional factors associated with indirect effects of pesticides on natural enemies
The methodology evaluates the indirect effects of pesticides on natural enemies that may influence the results obtained [136][137][138][139][140][141][142][143][144]. The indirect effects of pesticides against natural enemies not necessarily are affiliated with the active ingredient [136, [141-144]. It is can be formulations as emulsifiable concentrates (EC) and soluble powders (SP) contain additives as adjuvants, surfactants, solvents, or carriers that are indirectly harmful to natural enemies [145].

Summary
This chapter has demonstrated the feasibility of combining or integrating natural enemies with certain pesticides including systemic insecticides, insect growth regulators, selective feeding blockers, microbials, miticides, and fungicides. There are three primary means by which natural enemies integrated with pesticides including pesticide selection, spatial separation of natural enemies and pesticides, and temporal discontinuity between natural enemies and pesticides [114]. Indirect effects are evaluated to determine if pesticides are compatible with natural enemies [29]. Indirect effects depending on concentration, natural enemy species, pesticide exposure time, developmental life stage(s) evaluated, and the influence of residues and repellency [50].
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